Transvascular Delivery of Hydrophobically Modified siRNAs: Gene Silencing in the Rat Brain upon Disruption of the Blood-Brain Barrier

Mol Ther. 2018 Nov 7;26(11):2580-2591. doi: 10.1016/j.ymthe.2018.08.005. Epub 2018 Aug 8.

Abstract

Effective transvascular delivery of therapeutic oligonucleotides to the brain presents a major hurdle to the development of gene silencing technologies for treatment of genetically defined neurological disorders. Distribution to the brain after systemic administrations is hampered by the low permeability of the blood-brain barrier (BBB) and the rapid clearance kinetics of these drugs from the blood. Here we show that transient osmotic disruption of the BBB enables transvascular delivery of hydrophobically modified small interfering RNA (hsiRNA) to the rat brain. Intracarotid administration of 25% mannitol and hsiRNA conjugated to phosphocholine-docosahexanoic acid (PC-DHA) resulted in broad ipsilateral distribution of PC-DHA-hsiRNAs in the brain. PC-DHA conjugation enables hsiRNA retention in the parenchyma proximal to the brain vasculature and enabled active internalization by neurons and astrocytes. Moreover, transvascular delivery of PC-DHA-hsiRNAs effected Htt mRNA silencing in the striatum (55%), hippocampus (51%), somatosensory cortex (52%), motor cortex (37%), and thalamus (33%) 1 week after administration. Aside from mild gliosis induced by osmotic disruption of the BBB, transvascular delivery of PC-DHA-hsiRNAs was not associated with neurotoxicity. Together, these findings provide proof-of-concept that temporary disruption of the BBB is an effective strategy for the delivery of therapeutic oligonucleotides to the brain.

Keywords: RNA interference; hyperosmolar mannitol; intracarotid injection; osmotic disruption; therapeutic oligonucleotide.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / pathology
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / physiopathology
  • Brain / drug effects
  • Brain / physiopathology
  • Carotid Arteries / physiology
  • Docosahexaenoic Acids / administration & dosage
  • Docosahexaenoic Acids / chemistry
  • Gene Silencing
  • Genetic Therapy / methods
  • Humans
  • Huntingtin Protein / antagonists & inhibitors
  • Huntingtin Protein / genetics*
  • Hydrophobic and Hydrophilic Interactions
  • Mannitol / administration & dosage
  • Neurons / drug effects*
  • Neurons / pathology
  • Phosphorylcholine / administration & dosage
  • Phosphorylcholine / chemistry
  • RNA, Small Interfering / administration & dosage*
  • RNA, Small Interfering / chemistry
  • Rats

Substances

  • Htt protein, rat
  • Huntingtin Protein
  • RNA, Small Interfering
  • Phosphorylcholine
  • Docosahexaenoic Acids
  • Mannitol